Epigenetic Patterns and Geographical Parthenogenesis in the Alpine Plant Species Ranunculus kuepferi (Ranunculaceae)

Abstract

Polyploidization and the shift to apomictic reproduction are connected to changes in DNA cytosine-methylation. Cytosine-methylation is further sensitive to environmental conditions. We, therefore, hypothesize that DNA methylation patterns would differentiate within species with geographical parthenogenesis, i.e., when diploid sexual and polyploid apomictic populations exhibit different spatial distributions. On natural populations of the alpine plant Ranunculus kuepferi, we tested differences in methylation patterns across two cytotypes (diploid, tetraploid) and three reproduction modes (sexual, mixed, apomictic), and their correlation to environmental data and geographical distributions. We used methylation-sensitive amplified fragment-length polymorphism (methylation-sensitive AFLPs) and scored three types of epiloci. Methylation patterns differed independently between cytotypes versus modes of reproduction and separated three distinct combined groups (2x sexual + mixed, 4x mixed, and 4x apomictic), with differentiation of 4x apomicts in all epiloci. We found no global spatial autocorrelation, but instead correlations to elevation and temperature gradients in 22 and 36 epiloci, respectively. Results suggest that methylation patterns in R. kuepferi were altered by cold conditions during postglacial recolonization of the Alps, and by the concomitant shift to facultative apomixis, and by polyploidization. Obligate apomictic tetraploids at the highest elevations established a distinct methylation profile. Methylation patterns reflect an ecological gradient rather than the geographical differentiation.

Phenotypic Responses, Reproduction Mode and Epigenetic Patterns under Temperature Treatments in the Alpine Plant Species Ranunculus kuepferi (Ranunculaceae)

“…In case this phenotypic variation is heritable, DNA methylation could provide a mechanism of adaptive microevolution in plants [ 36 , 104 ], which is faster and independent from traditional genetic evolution [ 88 , 105 , 106 ]. Epigenetic variation differed in R. kuepferi between cytotypes, and also varied under climatic conditions, both in natural populations [ 68 ] and under controlled conditions [ 69 ].…”

“…A molecular dating revealed that the tetraploid cytotype originated only 10–80 thousand years ago [ 66 ], probably via multiple and recurrent polyploidization events [ 61 , 67 ]. Epigenetic studies using methylation-sensitive amplified fragment-length polymorphisms (MS-AFLPs) on the species suggested differential profiles in the cytotypes and a connection to abiotic environmental conditions of the epigenetic variation in natural populations and experimental treatments [ 68 , 69 ]. This epigenetic variation was further correlated with an elevation in natural populations [ 68 ] and showed higher persistence under cold treatment in experimental conditions [ 69 ].…”

“…Epigenetic studies using methylation-sensitive amplified fragment-length polymorphisms (MS-AFLPs) on the species suggested differential profiles in the cytotypes and a connection to abiotic environmental conditions of the epigenetic variation in natural populations and experimental treatments [ 68 , 69 ]. This epigenetic variation was further correlated with an elevation in natural populations [ 68 ] and showed higher persistence under cold treatment in experimental conditions [ 69 ]. Thus, we assume a putative epigenetic background of the niche shift of tetraploids in the Alps, which helps to understand the geographical parthenogenesis scenario for the species.…”

Chasing the Apomictic Factors in the Ranunculus auricomus Complex: Exploring Gene Expression Patterns in Microdissected Sexual and Apomictic Ovules

“…Likewise, observed variability of proportions of facultative apospory under different light stress conditions in hexaploid clone-mates of R. carpaticola × cassubicifolius , including residual levels in diploid and tetraploid cytotypes, suggests an influence of epigenetic regulatory mechanisms on reproductive phenotypes [ 45 , 46 ]. In R. kuepferi , differential cytosine-methylation patterns found in sexual and apomictic natural populations support this hypothesis [ 94 ]. In other apomictic plant groups different genes had been found linked to the apomixis phenotype or to individual components of apomixis (e.g., [ 95 , 96 , 97 , 98 , 99 , 100 , 101 ]).…”

Polyploidy Improves Photosynthesis Regulation within the Ranunculus auricomus Complex (Ranunculaceae)

“…Additionally, epigenetic control mechanisms may play a role. A study on cytosine methylation of diploid and tetraploid R. kuepferi revealed not only different methylation profiles between cytotypes, but also indicated two different epigenetic groups within tetraploids, correlating with different temperature exposures [ 69 ].…”